Ionic dependence of the velocity of release of ATP from permeabilized cholinergic synaptic vesicles

González-Sistal, À.; Reigada, David; Puchal, R.; Aranda, Inmaculada Gómez de; Elı́as, Marı́a Mónica; Marsal, Jordi; Solsona, Carles

doi:10.1016/j.neuroscience.2007.07.004

Cited by 10 publications

(8 citation statements)

References 11 publications

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“…Deconvolution analysis was performed as previously described (Gonzalez-Sistal et al, 2007). The light generated by the enzymatic reaction was transmitted through six optic fibers connected to a photomultiplier (R374; Hamamatsu Photonics, Spain) and controlled by a slit.…”

Section: Measurement Of Atp Release From Oocytesmentioning

confidence: 99%

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Role of connexin 32 hemichannels in the release of ATP from peripheral nerves

Nualart-Marti

Molino

Grandes

et al. 2013

Glia

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Extracellular purines elicit strong signals in the nervous system. Adenosine-5'-triphosphate (ATP) does not spontaneously cross the plasma membrane, and nervous cells secrete ATP by exocytosis or through plasma membrane proteins such as connexin hemichannels. Using a combination of imaging, luminescence and electrophysiological techniques, we explored the possibility that Connexin 32 (Cx32), expressed in Schwann cells (SCs) myelinating the peripheral nervous system could be an important source of ATP in peripheral nerves. We triggered the release of ATP in vivo from mice sciatic nerves by electrical stimulation and from cultured SCs by high extracellular potassium concentration-evoked depolarization. No ATP was detected in the extracellular media after treatment of the sciatic nerve with Octanol or Carbenoxolone, and ATP release was significantly inhibited after silencing Cx32 from SCs cultures. We investigated the permeability of Cx32 to ATP by expressing Cx32 hemichannels in Xenopus laevis oocytes. We found that ATP release is coupled to the inward tail current generated after the activation of Cx32 hemichannels by depolarization pulses, and it is sensitive to low extracellular calcium concentrations. Moreover, we found altered ATP release in mutated Cx32 hemichannels related to the X-linked form of Charcot-Marie-Tooth disease, suggesting that purinergic-mediated signaling in peripheral nerves could underlie the physiopathology of this neuropathy.

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Section: Measurement Of Atp Release From Oocytesmentioning

confidence: 99%

“…In divalent-free conditions, the Luciferase solution was prepared in a Ca 21free buffer containing 10 lM MgCl 2 to keep the enzyme active (Luciferase is Mg 21 dependent). Deconvolution analysis was performed as previously described (Gonzalez-Sistal et al, 2007).…”

Section: Measurement Of Atp Release From Oocytesmentioning

confidence: 99%

Role of connexin 32 hemichannels in the release of ATP from peripheral nerves

Nualart-Marti

Molino

Grandes

et al. 2013

Glia

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“…1997). Release of ACh and ATP was measured from permeabilized cholinergic synaptic vesicles from Torpedo marmorata electric organ and shown to be 10 times more effective in solutions containing Ca 2+ rather than Na + (Gonzalez‐Sistal et al. 2007).…”

Section: Lower Vertebratesmentioning

confidence: 99%

Evolutionary origins of the purinergic signalling system

2009

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Purines appear to be the most primitive and widespread chemical messengers in the animal and plant kingdoms. The evidence for purinergic signalling in plants, invertebrates and lower vertebrates is reviewed. Much is based on pharmacological studies, but important recent studies have utilized the techniques of molecular biology and receptors have been cloned and characterized in primitive invertebrates, including the social amoeba Dictyostelium and the platyhelminth Schistosoma, as well as the green algae Ostreococcus, which resemble P2X receptors identified in mammals. This suggests that contrary to earlier speculations, P2X ion channel receptors appeared early in evolution, while G protein-coupled P1 and P2Y receptors were introduced either at the same time or perhaps even later. The absence of gene coding for P2X receptors in some animal groups [e.g. in some insects, roundworms (Caenorhabditis elegans) and the plant Arabidopsis] in contrast to the potent pharmacological actions of nucleotides in the same species, suggests that novel receptors are still to be discovered.

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“…While mechanosensitive release of ATP from astrocytes is undoubtedly important, the enthusiasm accompanying the glial revolution may have overshadowed potential contributions from neurons. Classic vesicular release of ATP from the synaptic regions of neurons is well established (Gonzalez‐Sistal et al 2007), but release through non‐vesicular conduits has not been thoroughly studied. However, several observations suggest retinal ganglion cells are capable of mechanosensitive ATP release through non‐vesicular pathways.…”

Section: Introductionmentioning

confidence: 99%

Neurons respond directly to mechanical deformation with pannexin‐mediated ATP release and autostimulation of P2X₇ receptors

Xia

Lim

et al. 2012

The Journal of Physiology

143

163

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Key points• Neurons can be damaged when tissues are stretched or swollen; while astrocytes can contribute to this process, the mechanosensitive response from neurons is unclear.• We show here that isolated retinal ganglion cell neurons respond to mechanical strain with a rapid, sustained release of the neurotransmitter ATP.• The conduit for ATP release was through pannexin hemichannels, with probenicid, carbenoxelone and 10 panx inhibiting release.• Once released, this ATP acts back on the neurons to autostimulate lethal P2X 7 receptors, as A438079, AZ 10606120 and zinc reduced currents in whole cell patch clamp recordings.• Blocking release of ATP through pannexin channels, or activation of P2X 7 receptors, might be neuroprotective for stretched or swollen neurons.• Stretch-dependent release of ATP through neuronal pannexins, combined with the autostimulation of the P2X 7 receptors, provides a new pathway by which neuronal activity and health can be altered by mechanical strain independently of glial activity.Abstract Mechanical deformation produces complex effects on neuronal systems, some of which can lead to dysfunction and neuronal death. While astrocytes are known to respond to mechanical forces, it is not clear whether neurons can also respond directly. We examined mechanosensitive ATP release and the physiological response to this release in isolated retinal ganglion cells. Purified ganglion cells released ATP upon swelling. Release was blocked by carbenoxolone, probenecid or peptide 10 panx, implicating pannexin channels as conduits. Mechanical stretch of retinal ganglion cells also triggered a pannexin-dependent ATP release. Whole cell patch clamp recording demonstrated that mild swelling induced the activation of an Ohmic cation current with linear kinetics. The current was inhibited by removal of extracellular ATP with apyrase, by inhibition of the P2X 7 receptor with A438079, zinc, or AZ 10606120, and by pannexin blockers carbenoxolone and probenecid. Probenecid also inhibited the regulatory volume decrease observed after swelling isolated neurons. Together, these observations indicate mechanical strain triggers ATP release directly from retinal ganglion cells and that this released ATP autostimulates P2X 7 receptors. Since extracellular ATP levels in the retina increase with elevated intraocular pressure, and stimulation of P2X 7 receptors on retinal ganglion cells can be lethal, this autocrine response may impact ganglion cells in glaucoma. It remains to be determined whether the autocrine stimulation of J. Xia and J. C. Lim contributed equally to this work. purinergic receptors is a general response to a mechanical deformation in neurons, or whether preventing ATP release through pannexin channels and blocking activation of the P2X 7 receptor, is neuroprotective for stretched neurons.

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Ionic dependence of the velocity of release of ATP from permeabilized cholinergic synaptic vesicles

Cited by 10 publications

References 11 publications

Role of connexin 32 hemichannels in the release of ATP from peripheral nerves

Role of connexin 32 hemichannels in the release of ATP from peripheral nerves

Evolutionary origins of the purinergic signalling system

Neurons respond directly to mechanical deformation with pannexin‐mediated ATP release and autostimulation of P2X₇ receptors

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Ionic dependence of the velocity of release of ATP from permeabilized cholinergic synaptic vesicles

Cited by 10 publications

References 11 publications

Role of connexin 32 hemichannels in the release of ATP from peripheral nerves

Role of connexin 32 hemichannels in the release of ATP from peripheral nerves

Evolutionary origins of the purinergic signalling system

Neurons respond directly to mechanical deformation with pannexin‐mediated ATP release and autostimulation of P2X7 receptors

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Product

Resources

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Neurons respond directly to mechanical deformation with pannexin‐mediated ATP release and autostimulation of P2X₇ receptors